Skip to main content

Full text of "HIV Risky Sexual Behaviors and HIV Infection Among Immigrants: A Cross-Sectional Study in Lisbon, Portugal."

See other formats


Int. J. Environ. Res. Public Health 2014, 11, 8552-8566; doi:10.3390/ijerphl 10808552 



OPEN ACCESS 



International Journal of 
Environmental Research and 
Public Health 
ISSN 1660-4601 

www.mdpi.com/journal/ijerph 

Article 

HIV Risky Sexual Behaviors and HIV Infection Among 
Immigrants: A Cross-Sectional Study in Lisbon, Portugal 

Sonia Dias '*, Adilson Marques 2 , Ana Gama 1 and Maria O. Martins 1 

1 Instituto de Higiene e Medicina Tropical - Centro de Malaria e Outras Doencas Tropicais, 
Universidade Nova de Lisboa, Rua da Junqueira n° 100, Lisboa 1349-008, Portugal; 
E-Mails: anafgama@gmail.com (A.G.); mrfom@ihmt.unl.pt (M.O.M.) 

2 Faculdade de Motricidade Humana, Universidade de Lisboa, Estrada da Costa, 
Cruz Quebrada-Dafundo 1499-002, Portugal; E-Mail: amarques@fmh.ulisboa.pt 

* Author to whom correspondence should be addressed; E-Mail: smfdias@yahoo.com; 
sfdias@ihmt.unl.pt; Tel.: +351-213-652-600; Fax: +351-213-632-105. 

Received: 1 July 2014; in revised form: 23 July 2014 / Accepted: 12 August 2014 / 
Published: 20 August 2014 

Abstract: This study aimed to examine risky sexual behavior, its associated factors and 
HIV infection among immigrants. A participatory cross-sectional survey was conducted with 
1187 immigrants at the National Immigrant Support Centre, in Lisbon (52.2% female; 
34.0% Africans, 33.8% Brazilians, 32.2% Eastern Europeans). About 38% of participants 
reported >2 sexual partners in the previous year, 16.2% both regular and occasional sexual 
partners (last 12 months), 33.1% inconsistent condom use with occasional partners, and 
64% no condom use in the last sexual intercourse. Unprotected sex in the last sexual 
intercourse was more likely among women, Africans, those older, with elementary 
education, those married and those who didn't receive free condoms in the previous year. 
No condom use was less likely among those having only occasional sexual partners and 
both regular and occasional sexual partners. One third of participants had never been tested 
for HIV. Those never tested reported more frequently inconsistent condom use than those 
ever tested. Overall, 2.0% reported being HIV positive (2.5% of men; 4.4% of Africans); 
4.3% admitted having a STI in previous year. HIV-positive immigrants reported high-risk 
sexual behaviors. Tailored interventions to promote awareness of HIV serostatus among 
immigrants as well as culturally adapted risk reduction strategies should be strengthened. 



Int. J. Environ. Res. Public Health 2014, 11 

Keywords: immigrants; HIV infection; risky sexual behavior 



8553 



1. Introduction 

The HIV epidemic continues to be a major public health concern in the European Union [1,2]. 
Increased international migration, particularly from highly endemic countries, has been acknowledged 
as one of the major factors influencing the epidemiology of HIV in Europe and contributing to the 
changing pattern of HIV transmission in this region, where in the recent years sexually transmitted 
cases have been on the rise [3]. Estimates indicate that approximately 40% of the HIV diagnosed cases 
during 2007-201 1 in Europe were in migrants [1]. 

Migration had been recognized to be associated with increased high risk sexual behaviors [4,5]. 
Previous research indicate that a considerable amount of immigrants report to have multiple partners 
and to not use condom consistently with both occasional (casual partner with no committed 
relationship) and regular (main, stable partner) partners [6-9], which renders this population 
particularly at risk for HIV infection. Explanations of the increased vulnerability of immigrants to HIV 
infection include the long periods away from family and partners, the associated need to seek 
companionship to compensate for the alienating aspects of the migration experience and the fewer 
social controls on behavior [9,10], but also the experience of social exclusion and lack of legal 
protection that often translate in lesser means of protection and poorer health status [7,9], and barriers 
to health services (related to their legal status, socioeconomic conditions, language and cultural 
difference) [3,11-13]. 

Despite the evidence of disproportionate HIV risk among migrants and increasing numbers of 
immigrants in the European context, there are few studies aimed to examine the extent of HIV 
infection, risky sexual behavior and its determinants among these populations. Additionally, many 
immigrants have not even been systematically included in HIV surveillance systems, as undocumented 
and recent immigrants who are omitted in the population census and records. Also, many groups 
underuse health services where surveillance data is reported (mainly due to mistrust or lack of 
knowledge about services available and migrants' health rights). Furthermore, in many cases data are 
not collected in a way that allows disaggregated analysis (in many countries no data is collected on 
variables as country of birth or ethnic group) [14,15]. 

Knowledge on HIV infection and risk behavior among immigrants is greatly needed to inform HIV 
prevention and control national programs as well as to provide valuable evidence for appropriate 
interventions in this population. This is particularly relevant in Portugal as it is one of the countries 
presenting the largest burden of infection in Western Europe-data estimates that in 2011 it had one of 
the highest incidence rates (11.8 per 100,000 population; 17.2 per 100,000 males and 6.7 per 100,000 
females) and the second highest HIV prevalence (0.7% among adults aged 15-49 years old) in the 
European Region [16,17]. Also, in the last decades Portugal has received many immigrants (the 
foreign-born population represent 8.3% of the total population in Portugal), mainly from countries with 
high HIV prevalence as most Portuguese-speaking African countries, Eastern European countries and 
Brazil [17-19]. In 2012, 29.4% (228) of the newly diagnosed cases in Portugal referred to immigrants: 



Int. J. Environ. Res. Public Health 2014, 11 



8554 



66.4% from Sub-Saharan Africa, 20.0% from Latin America, 11.4% from Europe [20]. This study 
aimed to examine risky sexual behaviors, its associated factors and HIV infection among immigrants 
in the Lisbon Metropolitan Area. 

2. Methods 

2.1. Study Design and Population 

A cross-sectional survey was conducted with immigrants in the Lisbon Metropolitan Area. 
This area has currently the highest concentration of immigrant population in the country. Official data 
indicate that, in 2011, 44% of the immigrant population in Portugal resided in the Lisbon region 
(around 188,259 and an undetermined number of undocumented persons excluded in the official 
statistics) [21]. A participatory approach was used: representatives of governmental organizations 
(public health services), non-governmental organizations (NGOs) and associations of African, 
Brazilian and Eastern European immigrants (who work in outreach projects in the areas of health 
promotion, HIV prevention and social support with immigrant communities) actively collaborated in 
all phases of the study. 

2.2. Sampling and Data Collection 

The study sample included 1187 immigrants who were interviewed at the National Immigrant 
Support Centre (NISC) in Lisbon over a 1 month period (February) in 2011. The NISC is part of the 
High Commission for Immigration and Intercultural Dialogue. Within a friendly environment, 
it provides integrated answers to needs faced by immigrants residing in Portugal (e.g., regularization 
process, interaction with public services) regardless of legal status or any other criterion. It brings 
together in one place different public institutions in the areas of health, education, social security, 
employment and justice [22,23]. 

All immigrants who visited the NISC premises during working hours were approached and invited 
to participate. The inclusion criteria were being an immigrant, defined as a non-national person who 
migrated to Portugal for the purpose of settlement [24], and being >18 years old. The proportion of 
refusals was 9.7% (n = 127; 57.7% were female). No further information was collected from those 
who refused. 

Data were collected through an anonymous structured questionnaire. Given the sensitive nature of 
the subject under investigation, the interviews took place in a quiet and isolated room at NISC offices 
to ensure privacy and comfort of participants. The questionnaire was applied by trained interviewers 
from immigrant communities, recruited and selected in collaboration with NGOs and immigrant 
associations. Interviews were applied in Portuguese — it is the official language of Africans and 
Brazilians in Portugal and many Eastern Europeans are fluent in Portuguese. In the few cases of 
Eastern Europeans who weren't fluent in Portuguese, specific interviewers applied the questionnaire in 
the native language. The questionnaire was administered using pen and paper. The interviewers 
training included information about the questionnaire, the data collection procedures and general 
interview techniques. 



Int. J. Environ. Res. Public Health 2014, 11 



8555 



Anonymous participation and confidentiality of data was guaranteed. Informed consent was 
obtained. The study was approved by the Ethical Committee of Instituto de Higiene e Medicina 
Tropical, Universidade Nova de Lisboa. 

2.3. Instrument 

The questionnaire comprised items on socio demo graphic characteristics, sexual behaviors, 
HIV testing, self-reported HIV infection and other STI, use of health services and prevention 
initiatives. In more detail: 

Sociodemographic characteristics: These included sex, age (continuous variable), educational level 
("elementary", "secondary", "higher"), marital status ("single", "married", "divorced or separated" and 
"widowed"; for analysis these options were dichotomized into "unmarried" — single/divorced or 
separated/widowed — and "married"), professional situation ("employed part-time", "employed full-time", 
"working-student", "student", "unemployed" and "retired"; for analysis these options were dichotomized 
into "non-employed" — student/unemployed/retired-and "employed"-employed part-time/employed 
full-time/working-student), perceived monthly income ("very insufficient", "insufficient", "sufficient" 
and "more than sufficient"; for analysis these options were dichotomized into "insufficient" and 
"sufficient"), and migration-related characteristics such as origin (response options included a list of 
countries which were then aggregated into "African", "Brazilian" and "Eastern European"), length of 
stay (in months for those residing in Portugal for <1 year, and in years for those residing for >1 year) 
and immigration status ("undocumented", "documented"). 

Sexual behaviors: Participants were asked about age at first sexual intercourse (in years); 
engagement in sexual intercourse (yes/no), number and type of sexual partners, commercial sex 
(yes/no), sex with a same-sex partner (yes/no) and condom use by type of sexual partner in the 
reference period of 12 months; type of sexual partner and condom use in the last sexual intercourse. 
Regarding type of sexual partner, two response options were used (regular/occasional partner) — 
regular sexual partner was defined as a person with whom one has sexual intercourse and has plans for 
further long term or committed relationship; occasional sexual partner was defined as a person with 
whom one has sexual intercourse (without payment) and has no plans for further long term or 
committed relationship [8]. As these response options were not mutually exclusive, for the analysis they 
were categorized into "only regular", "only occasional" and "regular and occasional". Engagement in 
commercial sex was defined as having had sexual intercourse with a person involving money or goods 
exchange between the two parties [25]. Regarding condom use in the last 12 months, participants were 
asked how often a condom was used (by him/herself or his/her sexual partner) during their sexual 
relations, having three possible response options (always/sometimes/rarely or never). For analysis this 
variable was dichotomized into consistent (always) and inconsistent (sometimes/rarely or never) condom 
use. Participants were also asked whether a condom was used (by him/herself or his/her sexual partner) 
in their last sexual intercourse, being the possible response options "yes" and "no". 

HIV testing: Participants provided information on whether they had been tested for HIV ever and in 
the previous 12 months, both questions with "yes'V'no" response options. 



Int. J. Environ. Res. Public Health 2014, 11 



8556 



HIV/STI status: Participants were asked to self-report their current serostatus for HIV and their 
serostatus for other sexually transmitted infections (STIs) in the last 12 months. 

Use of health services and prevention initiatives: Participants were asked about ever use of health 
services in Portugal, ever attendance of a sexual and reproductive health consultation and having 
received free condoms in the previous 12 months, all with "yes'V'no" response options. 

The questionnaire was designed in order to provide data for the second generation indicators created 
in accordance with international guidelines [26,27]. The items used in the questionnaire were also 
based on other international HIV research projects on migrants [28-30]. The instrument was 
constructed along with feedback provided by the partners of the study. The questionnaire was 
pre-tested with members of immigrant communities; few amendments were made to improve clarity 
and appropriateness of the questions to the study populations. 

2.4. Data Analysis 

Data analysis was performed using IBM SPSS Statistics v.22. The bivariate associations between 
sociodemographic characteristics, migration-related variables, sexual behaviors, HIV testing, self-reported 
infection, use of health services, prevention initiatives and gender were assessed using x, 2 and Fisher's 
exact tests when appropriate. Logistic regression analyses were performed to estimate the crude odds 
ratios (OR), adjusted OR and 95% confidence intervals (CI) of factors associated with no condom use 
in the last sexual intercourse. For analysis of sexual behaviors in the previous 12 months, 176 participants 
were excluded as they haven't reported sexual intercourse during this period. 

3. Results 

3.1. Characteristics of Participants 

The socio-demographic and migration-related characteristics of the male and female participants are 
shown in Table 1. In brief, 52.2% of the sample was female. Approximately two thirds of the 
participants were 25-44 years old. Overall, 34% were Africans (from Portuguese-speaking African 
countries: Angola, Cape Verde, Guinea Bissau, Mozambique, and Sao Tome and Principe), 33.8% 
were Brazilians and 32.2% Eastern Europeans (from Ukraine, Moldavia, Russia, Romania, Belarus and 
Bulgaria). About 38% had secondary education, more men than women (p = 0.028). More than a half 
of participants were not married. A third reported being undocumented, 47.1% were non-employed 
and 57.6% perceived their monthly income as insufficient. Mean length of stay in Portugal was 
7.5 years (±7.5). 

Table 1. Socio-demographic and migration-related characteristics by gender. 

Total Men Women p " 

n % n % n % 

1187 100 567 47.8 620 52.2 

0.173 

189 15.9 101 17.8 88 14.2 

751 63.3 356 62.8 395 63.7 

247 20.8 110 19.4 137 22.1 



Total 

Age (years) (n = 1 187) 
18-24 
25-44 
45-65 



Int. J. Environ. Res. Public Health 2014, 11 



8557 



Table 1. Cont. 



Total Men Women p" 





n 


% 


n 


% 


n 


% 




Origin (n= 1187) 














0.997 


Eastern European 


383 


32.2 


183 


32.3 


200 


32.2 




Brazilian 


401 


33.8 


191 


33.7 


210 


33.9 




African 


403 


34.0 


193 


34.0 


210 


33.9 




Educational level (n = 1 1 82) 














0.028 


Higher 


419 


35.4 


187 


33.2 


232 


37.5 




Secondary 


448 


37.9 


236 


41.8 


212 


34.3 




Elementary 


315 


26.6 


141 


25.0 


174 


28.2 




Marital status (« = 1184) 














0.457 


Unmarried 


723 


61.1 


340 


60.0 


383 


62.1 




Married 


461 


38.9 


227 


40.0 


234 


37.9 




Immigration status (n = 1 176) 














0.084 


Undocumented 


390 


33.2 


200 


35.7 


190 


30.9 




Documented 


786 


66.8 


361 


64.3 


425 


69.1 




Professional status (n = 1 1 87) 














0.905 


Non-employed 


559 


47.1 


266 


46.9 


293 


47.3 




Employed 


628 


52.9 


301 


53.1 


327 


52.7 




Perceived monthly income [n = 1 1 84) 














0.904 


Insufficient 


682 


57.6 


325 


57.4 


357 


57.8 




Sufficient 


502 


42.4 


241 


42.6 


261 


42.2 






Mean ± SD 


Mean ± SD 


Mean ± SD 


P h 


Length of stay in Portugal (years) (n = 1181) 


7.5 ±7.5 


7.8 


±7.9 


7.2 ±7.1 


0.200 



Tested by Chi-square or Exact Fisher Test; b Tested by T-test. 



3.2. Risk Sexual Behaviors, HIV Testing and HIV Infection 

Table 2 presents the data on risk sexual behaviors, HIV testing and reported HIV infection of the 
participants stratified by gender. Compared to women, men reported lower mean age at first sexual 
intercourse and higher number of sexual partners in the last year. Also, a higher proportion of men 
reported having both regular and occasional sexual partners in the last year and having their most 
recent sexual intercourse with an occasional partner. Also, a higher proportion of men reported 
engagement in sexual intercourse with same-sex partners and in commercial sex in the previous year, 
comparing to women. 

Condom use with occasional partners in the last 12 months was inconsistent among 33.1% of 
participants, significantly more women than men (44.8% and 28.7%, respectively). Inconsistent 
condom use with regular partners was reported by 81.7% of participants, with no significant 
differences across gender. About 73% of women and 54.2% of men didn't use condom at their most 
recent sexual intercourse. 

Approximately 38% of participants reported having never been tested for HIV, more men than 
women; of those ever tested, 63.4% were not tested in the last year. Those never tested reported more 
frequently inconsistent condom use with occasional partners (42.7% compared to 28.9% of those ever 
tested for HIV, p = 0.034) and with regular partners (85.2% vs. 79.8% of those ever tested for HIV, 
/? = 0.05). 



Int. J. Environ. Res. Public Health 2014, 11 



8558 



Table 2. Risk sexual behaviors, HIV testing, reported HIV infection, use of health services 
and prevention initiatives by gender. 



Total Men Women 





Mean ± SD 


Mean ± SD 


Mean ± SD 


P* 


Age at first sexual intercourse (n = 975) 


16.9 ±2.9 


16.2 ±2.9 


17.5 ±2.8 


<0.001 




n 


% 


n 


% 


n 


% 


h 

p 


Number of sexual partners in the previous 














<0.001 


12 months (n = 974) 














1 partner 


604 


62.0 


233 


50.0 


371 


73.0 




2-3 partners 


256 


26.3 


147 


31.5 


109 


21.5 




> 4 partners 


114 


11.7 


86 


18.5 


28 


5.5 




Type of sexual partners in the previous 














<0.001 


12 months (n = 998) 














Only regular 


737 


73.8 


284 


59.9 


453 


86.5 




Only occasional 


99 


9.9 


77 


16.2 


22 


4.2 




Regular and occasional 


162 


16.2 


113 


23.8 


49 


9.4 




Sexual intercourse with same-sex partners in 














0.007 


the previous 12 months (n = 1002) 














No 


943 


94.1 


437 


92.0 


506 


96.0 




Yes 


59 


5.9 


38 


8.0 


21 


4.0 




Commercial sex in the previous 12 months (n = 1011) 














0.002 


No 


972 


96.1 


450 


94.1 


522 


97.9 




Yes 


39 


3.9 


28 


5.9 


11 


2.1 




Type of sexual partner at the most recent sexual 














<0.001 


intercourse (n = 1008) 














Regular 


827 


82.0 


348 


73.0 


479 


90.2 




Occasional 


181 


18.0 


129 


27.0 


52 


9.8 




Condom use with regular partners in the 














0.068 


previous 12 months (n = 890) 














Consistent 


163 


18.3 


83 


21.0 


80 


16.2 




Inconsistent 


727 


81.7 


313 


79.0 


414 


83.8 




Condom use with occasional partners in the previous 














0.017 


12 months (n = 248) 














Consistent 


166 


66.9 


129 


71.3 


37 


55.2 




Inconsistent 


82 


33.1 


52 


28.7 


40 


44.8 




Condom use in the last sexual encounter (n = 992) 














<0.001 


No 


635 


64.0 


254 


54.2 


381 


72.8 




Yes 


357 


36.0 


215 


45.8 


142 


27.2 




Ever testing for HIV (n = 1 185) 














O.001 


Yes 


740 


62.4 


316 


55.8 


424 


68.5 




No 


445 


37.6 


250 


44.2 


195 


31.5 




Reported HIV status (n = 735) 1 














0.407 


Negative 


720 


97.3 


307 


97.5 


413 


98.3 




Positive 


15 


2.0 


8 


2.5 


7 


1.7 




Ever utilization of health services in Portugal (n = 1 186) 














<0.001 


No 


207 


17.5 


125 


22.0 


82 


13.2 




Yes 


979 


82.5 


442 


78.0 


537 


86.8 




Attendance to a sexual and reproductive 














<0.001 


consultation (n = 1 169) 














No 


876 


74.9 


489 


87.6 


387 


63.3 




Yes 


293 


25.1 


69 


12.4 


224 


36.7 




Free condoms received in the previous 














0.047 


12 months (n =1186) 














Yes 


391 


33.0 


203 


35.8 


188 


30.4 




No 


795 


67.0 


364 


64.2 


431 


69.6 





1 For the analyses it was only considered participants who reported to have been tested for HIV; a Tested by T-test; 
b Tested by Chi -square or Exact Fisher Test. 



Int. J. Environ. Res. Public Health 2014, 11 



8559 



Of those ever tested for HIV, 15 participants (2.0%) reported being HIV positive: 2.5% of men and 
1.7% of women; 4.4% (n = 12) of Africans, 1.2% {n = 2) of Eastern Europeans and 0.3% {n = 1) of 
Brazilians (data not shown in the table). HIV-positive participants reported high-risk sexual behaviors: 
nine participants (60.0%) had two or more sexual partners in the last year, six (40.0%) had occasional 
sexual partners and three (20.0%) both regular and occasional sexual partners in the last year, four 
(26.7%) inconsistently used condom with occasional partners and four (26.7%) with regular partners. 
No significant differences were found across gender and origin. 

Overall, 4.3% (n = 50) of participants admitted having a STI in the previous year: 5.1% (n = 31) of 
women and 3.5% (n = 19) of men; 6.1% (n = 24) of Africans, 4.0% (n = 16) of Brazilians and 2.8% 
(n = 10) of Eastern Europeans. 

3. 3. Use of Health Services and Preventive Initiatives 

Table 2 also shows the distribution of ever use of health services, attendance to a sexual and 
reproductive health consultation and free condoms received by gender. A significantly higher 
proportion of women reported having ever used the health services and having attended a sexual and 
reproductive health consultation, while men reported more frequently having received free condoms in 
the previous year. Participants who ever used health services reported more frequently having been 
tested for HIV compared to those who never used (64.5% vs. 52.7%, p = 0.001). Similar result was 
found for attending a sexual and reproductive health consultation (74.7% among those who had 
attended vs. 58.6% of those who never attended, p < 0.001) (data not shown). 

3. 4. Factors Associated with no Condom Use in the Last Sexual Intercourse 

Logistic regression estimation results for factors associated with the likelihood of not having used 
condom in the last sexual intercourse are presented in Table 3. After adjusting the logistic regression 
model to all variables presented in the analysis, having not used condom was more likely among 
women (OR = 1.73, 95% CI: 1.25-2.40), Africans (OR = 1.81, 95% CI: 1.11-2.96) compared to 
Eastern Europeans, those older (OR = 1.84, 95% CI: 1.02-3.32), those with elementary education 
(OR = 1.84, 95% CI: 1.11-3.01) compared to higher education, those married (OR = 2.38, 95% CI: 
1.67-3.38) and those who didn't receive free condoms in the previous year (OR = 1.49, 95% 
CI: 1.06-2.09). No condom use was less likely among immigrants who had only occasional sexual 
partners (OR = 0.10, 95% CI: 0.05-0.20) and both regular and occasional sexual partners (OR = 0.43, 
95% CI: 0.25-0.75). 

Table 3. Logistic regression results for factors associated with no condom use in the last 
sexual intercourse. 



«(%)(« = 635) Crude OR (95% CI) Adjusted OR (95% CI) 



Sex 

Male 

Female 
Origin 

Eastern European 



254 (54.2) 
381 (72.8) 



184 (64.3) 



1.00 

2.27 (1.74-2.96) *** 



1.00 



1.00 

1.73 (1.25-2.40) ** 



1.00 



Int. J. Environ. Res. Public Health 2014, 11 



8560 



Table 3. Cont. 





n (%) (« = 635) 


Crude OR (95% CI) 


Adjusted OR (95% CI) 1 


Brazilian 


215 (57.5) 


0.75 (0.55-1.03) 


1.05 (0.68-1.61) 


African 


236 (71.1) 


1.36 (0.97-1.91) 


1.81 (1.11-2.96)* 


Age (years) 








18-24 


78 (50.0) 


1.00 


1.00 


25-44 


418 (63.5) 


1.74(1.23-2.48) ** 


1.20 (0.77-1.87) 


45-65 


139 (78.1) 


3.56 (2.22-5.73) *** 


1.84(1.02-3.32)* 


Educational level 








Higher 


206 (61.9) 


1.00 


1.00 


Secondary 


235 (59.0) 


0.89 (0.66-1.20) 


1.40 (0.95-2.07) 


Elementary 


191 (74.3) 


1.78 (1.25-2.55) ** 


1.84(1.11-3.01) * 


Marital status 








Unmarried 


301 (52.8) 


1.00 


1.00 


Married 


332 (79.0) 


3.37 (2.53-4.49) *** 


2.38 (1.67-3.38) *** 


Number of sexual partners 








1 partner 


447 (75.4) 


1.00 


1.00 


2-3 partners 


138 (54.3) 


0.39 (0.29-0.53) *** 


0.94 (0.60-1.48) 


>4 partners 


31 (27.7) 


0.13 (0.08-0.20) *** 


0.76 (0.38-1.50) 


Type of sexual partners in the 








previous 12 months 








Only regular 


546 (75.6) 


1.00 


1.00 


Only occasional 


14(14.1) 


0.05 (0.03-0.10) *** 


0.10 (0.05-0.20) *** 


Regular and occasional 


71 (44.7) 


0.26 (0.18-0.37) *** 


0.43 (0.25-0.75) ** 


Free condoms received in the 








previous 12 months 








Yes 


184 (51.8) 


1.00 


1.00 


No 


451 (70.8) 


2.25 (1.72-2.95) *** 


1.49(1.06-2.09) ** 


Ever testing for HIV 








Yes 


410 (62.6) 


1.00 


1.00 


No 


225 (66.8) 


1.20 (0.91-1.58) 


1.13 (0.80-1.59) 



1 Adjusted for sex, origin, age, educational level, marital status, number of sexual partners, type of sexual partners in the 
previous 12 months, free condoms received in the previous 12 months and ever testing for HIV. * p < 0.05; ** p < 0.01; 
"'p< 0.001. 



4. Discussion 

In general, the results of this study indicate high rates of risky sexual behaviors among immigrants, 
including having multiple (concurrent) sexual partners and unprotected sexual intercourse, consistently 
with other research conducted in Europe [6,31] and in other regions [9,29,32,33]. These findings 
highlight the potential increasing risk for HIV infection of migrants who have unprotected sex with 
multiple sexual partners, but also if they acquire HIV/AIDS the increasing likelihood of transmitting 
HIV infection to their partners. 

As would be expected, we found wide variability in sexual risk behaviors across gender. Women 
reported significantly less condom use than men. This can be strongly related to gender power 
inequalities and lack of negotiating capacity to request safer sex, which renders women particularly 
vulnerable to partners' risk behaviors [34,35]. On the other hand, although consistent condom use was 
more frequent among men, the reported higher rates of multiple sexual partners, engagement in 



Int. J. Environ. Res. Public Health 2014, 11 



8561 



commercial sex and with same-sex partners puts this subgroup at increased risk for HIV infection. 
A key element to be explored in future research is the variations in the pattern of risk practices through 
the different phases of the migration process and within each geographic context. 

The overall reported HIV prevalence in this study was 2% and 4.4% in the African subgroup, much 
higher compared to that estimated for the general national population (0.7% among individuals aged 
15-49 years) [17]. The scant published research in the European context show relatively great levels of 
infection. In a cross-sectional survey conducted in London with a convenience sample of Central and 
Eastern European migrants, 1.1% of respondents reported being HIV positive [6]. A study carried out 
in HIV counselling and testing clinics in several Spanish cities included a sample of immigrants who 
voluntarily tested for HIV and the HIV prevalence obtained ranged from 1.7% in Central and Eastern 
Europeans and in Latin Americans, 2.4% in North Africans and 8.4% in Sub-Saharan Africans [36]. 
In other cross-sectional community-based survey conducted with 1006 black- Africans in England, 
14% of participants tested HIV positive [30]. Given that our data is solely based on self-reported 
information with absence of biological samples, we can speculate that the proportion of HIV-positive 
immigrants among our sample is probably higher. 

The greater prevalence of HIV among African immigrants found in our sample has also been 
described in other European studies [30,36-38]. This certainly can be related to the higher prevalence 
of HIV in their countries of origin but also to their greater exposure to HIV risk. Indeed, African 
immigrants reported higher rates of risk sexual behaviors (multiple sexual partners, concomitant 
partners in the last year and inconsistent condom use-from further analysis not shown). In future 
research it is essential to further explore the patterns of risk behaviors of migrants and the underlying 
individual, sociocultural and contextual factors as also the epidemiological background. 

A relevant result in our study is the observation of risky sexual behaviors among HIV-positive 
immigrants. Although caution is needed when analyzing the results because the sample size is small, a 
relatively large proportion of these participants reported having multiple sexual partners, having both 
regular and occasional partners in the previous year and engaging in unprotected sex, which poses 
direct risks for HIV transmission. Secondary prevention strategies are warranted to foster safer sex 
practices among those living with HIV. 

It is also important to point out the high reported prevalence of STI found in this study. There is 
clear evidence that STI increase the likelihood of HIV transmission and similar sexual behaviors place 
people at high risk of both infections [39]. Our findings reinforce the need of strengthening integrated 
HIV and STI prevention and control programs among immigrants. 

Approximately 38% of immigrants in this study reported having never been tested for HIV and of 
those who ever tested, 63.4% were not tested in the last year. These may include a potential group of 
immigrants with undiagnosed HIV infection. Moreover, immigrants who never tested for HIV reported 
more frequently risky sexual behavior. Evidence gained in continued experience in HIV testing 
indicates that increasing individuals' awareness of HIV infection and counseling them to develop 
appropriate sexual protective measures leads to substantial reductions in high-risk sexual 
behavior [40-42]. Therefore, promotion of HIV testing among this population should be sustained. 

When promoting HIV testing it must be taken into account the important finding observed in this 
study and in other research that having never been tested for HIV is significantly associated with 
having never used health services or attended a sexual reproductive health consultation [43,44]. 



Int. J. Environ. Res. Public Health 2014, 11 



8562 



Our results show a considerable proportion of immigrants who never used the health services, in line 
with previous studies [45-48]. Although no specific data were collected on barriers in utilization of 
health services, the literature points out migrants' lack of knowledge on the health services available, 
the lack of cultural competence of health professionals and structural barriers as cost, distance of 
health services and legal restrictions [12,46,49,50]. These findings support the need to overcome 
barriers and promote the use of health services in order to reduce missed opportunities for early 
detection of HIV and prevention among this population. 

Immigrants who received free condoms were less likely to had unprotected sex, suggesting that the 
provision of free condoms to other immigrants can have the same benefits. Additionally, we found a 
relationship between low educational level and having not used condom in the last sexual intercourse. 
A possible explanation is that lower educational level, frequently related to the lack of knowledge on 
HIV transmission and prevention, may hinder risk perception and increase the adoption of unsafe 
sexual practices [8,25,51,52]. Community-based initiatives promoted by outreach teams who have 
trusting relationships with the community and have unique knowledge of its context can contribute to 
promote effective HIV prevention interventions among these populations [10,53]. 

The findings must be interpreted with consideration of some limitations. The cross-sectional nature 
of the data limits our ability to draw causal inferences. Another limitation relates to the sampling 
procedure. Although the study achieved a diverse and large sample we did not use a random sampling 
method to select the study population. In fact, the information available on immigrant population in 
Portugal does not allow constructing sampling frames for representative population-based surveys that 
capture hard-to-reach subgroups as undocumented and recent immigrants. Collecting data only from 
migrants presenting themselves at the NISC potentially leads to an overrepresentation of more affluent 
and better integrated migrant groups. However, as this center is viewed by immigrants as an 
independent institution dedicated to solving individual integration problems, we are confident that the 
sampling procedure allowed for a fairly representative sample of migrant conditions. Also, the participants' 
socio-demographic profiles are in line with data on immigrant populations in Portugal [19]. We did not 
collect data on reasons for refusals, but the topic explored in this study may have motivated individuals 
to refuse, which could mask a higher prevalence of risk behaviors and infection among this population. 
As in many other investigations, another limitation is the collected information based on self-reports. 
Due to the intimate and sensitive nature of the study subject and the high degree of stigma and 
discrimination attached to risky sexual behavior and HIV/STI positive serostatus, response bias toward 
under-reporting in this study would be expected. 

Despite study limitations, this large-scale study provides useful insights on risky sexual behavior 
and HIV infection/STI among immigrants. In order to improve our understanding of the complex 
dynamics of HIV risk and infection in this population further research is needed. 

5. Conclusions 

In summary, this study shows that a considerable proportion of immigrants engage in risky sexual 
behaviors rendering them at high risk for HIV infection. Our findings highlight that efforts to promote 
HIV testing and awareness of HIV serostatus among immigrants as well as culturally adapted 
interventions promoting risk reduction strategies should be strengthened. Given the enormous 



Int. J. Environ. Res. Public Health 2014, 11 



8563 



heterogeneity of immigrant communities, tailored interventions should be developed targeting subgroups 
prone to high risk sexual behaviors and matching their specific prevention needs. 

Acknowledgments 

This work was partially supported by National Coordination for HIV/AIDS Infection. We wish to 
thank all participants of this study. We are very grateful to all the community partners of the project. 
We also would like to acknowledge the commitment of the team of interviewers who were responsible 
for the collection of the study data. 

Author Contributions 

Sonia Dias and Ana Gama designed the study and coordinated the data collection process. Adilson 
Marques and Maria O. Martins were responsible for all statistical analyses. All authors wrote, 
reviewed the manuscript and approved the final version. 

Conflicts of Interest 

The authors declare no conflict of interest. 
References 

1. ECDC. Assessing the Burden of Key Infectious Diseases Affecting Migrant Populations in the 
EU/EEA-Executive Summary; ECDC: Stockholm, Sweden, 2014. 

2. Likatavicius, G.; van de Laar, M. HIV and AIDS in the European Union, 2011. Euro Surveill. 
2012, 17. Available online: http://www.eurosurveillance.org/View Article. aspx?ArticleId=20329 
(accessed on 12 December 2012). 

3. ECDC. Migrant Health: Epidemiology of HIV and AIDS in Migrant Communities and Ethnic 
Minorities in EU/EEA Countries; ECDC: Stockholm, Sweden, 2010. 

4. Dosekun, O.; Fox, J. An overview of the relative risks of different sexual behaviours on HIV 
transmission. Curr. Opin. HIV AIDS 2010, 5, 291-297. 

5. Gilbart, V.L.; Mercer, C.H.; Dougan, S.; Copas, A.J.; Fenton, K.A.; Johnson, A.M.; Evans, B.G. 
Factors associated with heterosexual transmission of HIV to individuals without a major risk 
within England, Wales, and Northern Ireland: A comparison with national probability surveys. 
Sex. Transm. Infect. 2006, 82, 15-20. 

6. Burns, F.M.; Evans, A.R.; Mercer, C.H.; Parutis, V.; Gerry, C.J.; Mole, R.C.M.; French, R.S.; 
Imrie, J.; Hart, G.J. Sexual and HIV risk behaviour in central and eastern European migrants in 
London. Sex. Transm. Infect. 2011, 87, 318-324. 

7. Sanchez, M.A.; Hernandez, M.T.; Hanson, J.E.; Vera, A.; Magis-Rodriguez, C; Ruiz, J.D.; 
Garza, A.H.; Castaneda, X.; Aoki, B.K.; Lemp, G.F. The effect of migration on HIV high-risk 
behaviors among Mexican migrants. J. Acquir. Immune Defic. Syndr. 2012, 61, 610-617. 

8. Wang, K.-W.; Wu, J.-Q.; Zhao, H.-X.; Li, Y.-Y.; Zhao, R; Zhou, Y; Ji, H.L. Unmarried male 
migrants and sexual risk behavior: A cross-sectional study in Shanghai, China. BMC Public Health 
2013, 13, doi:10. 1 186/1471-2458-13-1 152. 



Int. J. Environ. Res. Public Health 2014, 11 



8564 



9. Wu, J.-Q.; Wang, K.-W.; Zhao, R.; Li, Y.-Y.; Zhou, Y.; Li, Y.-R.; Ji, H.L.; Ji, M. 
Male rural-to-urban migrants and risky sexual behavior: A cross-sectional study in Shanghai, China. 
Int. J. Environ. Res. Public Health 2014, 11, 2846-2864. 

10. Hernandez, M.T.; Lemp, G.F.; Castaneda, X.; Sanchez, M.A.; Aoki, B.K.; Tapia-Conyer, R; 
Drake, M.V. HIV/AIDS among Mexican migrants and recent immigrants in California and Mexico. 
J. Acquir. Immune Defic. Syndr. 2004, 37, s203-s217. 

11. Dias, S.; Gama, A.; Rocha, C. Immigrant women's perceptions and experiences of health care 
services: Insights from a focus group study. J. Public Health 2010, 18, 489-496. 

12. Scheppers, E.; van Dongen, E.; Dekker, J.; Geertzen, J.; Dekker, J. Potential barriers to the use of 
health services among ethnic minorities: A review. Fam. Pract. 2006, 23, 325-348. 

13. WHO; UNAIDS; UNICEF. Global HIV/AIDS Response: Epidemic Update and Health Sector 
Progress towards Universal Access; WHO: Geneva, Switzerland, 2011. 

14. Del Amo, J.; Broring, G.; Hamers, F.; Infuso, A.; Fenton, K. Monitoring HIV/AIDS in Europe's 
migrant communities and ethnic minorities. AIDS 2004, 18, 1867-1873. 

15. Salama, P.; Dondero, T.J. HIV surveillance in complex emergencies. AIDS 2001, 15, S4-S12. 

16. ECDC/WHO. HIV/AIDS Surveillance in Europe 2012; ECDC: Stockholm, Sweden, 2013. 

17. UNAIDS. UNAIDS Report on the Global AIDS Epidemic 2012; UNAIDS: Geneva, 
Switzerland, 2012. 

18. OECD. International Migration Outlook 2013— OECD READ Edition; OECD: Paris, France, 2013. 

19. SEF. Relatdrio de Imigraqao, Fronteiras e Asilo-2013; SEF: Lisboa, Portugal, 2014. 

20. INSA. Infeqao VIH/SIDA: A Situaqao em Portugal a 31 de Dezembro de 2012; INSA: 
Lisboa, Portugal, 2013. 

21 . SEF. Relatdrio de Imigraqao, Fronteiras e Asilo-2011; SEF: Lisboa, Portugal, 2012. 

22. ACIDI. Handbook on How to Implement a One-Stop-Shop; ACIDI: Lisbon, Portugal, 2009. 

23. Niessen, J.; Schibel, Y. Handbook on Integration for Policy-makers and Practitioners; 
European Commission: Brussels, Luxembourg, 2004. 

24. IOM. International Migration Law: Glossary on Migration; IOM: Geneva, Switzerland, 2004. 

25. Wang, Y.; Cochran, C; Xu, P.; Shen, J.J.; Zeng, G; Xu, Y.; Sun, M.; Li, C; Li, X.; Chang, F.; et al. 
Acquired immunodeficiency syndrome/human immunodeficiency virus knowledge, attitudes, 
and practices, and use of healthcare services among rural migrants: A cross-sectional study in 
China. BMC Public Health 2014, 14, 158. 

26. ECDC. Mapping of HIV/STI Behavioural Surveillance in Europe; ECDC: Stockholm, Sweden, 2009. 

27. UNAIDS. Monitoring the Declaration of Commitment on HIV/AIDS-Guidelines on Construction 
of Core Indicators 2010 Reporting; UNAIDS: Geneva, Switzerland, 2009. 

28. Evans, A.R.; Parutis, V.; Hart, G; Mercer, C.H.; Gerry, C; Mole, R.; French, R.S.; Imrie, J.; 
Burns, F. The sexual attitudes and lifestyles of London's Eastern Europeans (SALLEE Project): 
Design and methods. BMC Public Health 2009, 9, doi:10.1 186/1471-2458-9-399. 

29. Lurie, M.N.; Williams, B.G.; Zuma, K.; Mkaya-Mwamburi, D.; Garnett, G.; Sturm, A.W.; 
Sweat, M.D.; Gittelsohn, J.; Addool Karim, S.S. The impact of migration on HIV-1 transmission 
in South Africa: A study of migrant and nonmigrant men and their partners. Sex. Transm. Dis. 
2003, 30, 149-156. 



Int. J. Environ. Res. Public Health 2014, 11 



8565 



30. Sadler, K.E.; McGarrigle, C.A.; Elam, G.; Ssanyu-Sseruma, W.; Davidson, O.; Nichols, T.; 
Mercey, D.; Parry, J.V.; Fenton, K.A. Sexual behaviour and HIV infection in black- Africans in 
England: Results from the Mayisha II survey of sexual attitudes and lifestyles. Sex. Transm. Infect. 
2007, 83, 523-529. 

31. Gras, M.; van Benthem, B. Determinants of high-risk sexual behavior among immigrant groups in 
Amsterdam: Implications for interventions. J. Acquir. Immune Defic. Syndr. 2001, 28, 166-172. 

32. Saggurti, N.; Verma, R.K.; Jain, A.; RamaRao, S.; Kumar, K.A.; Subbiah, A.; Modugu, H.R; 
Halli, S.; Bharat, S. HIV risk behaviours among contracted and non-contracted male migrant 
workers in India: Potential role of labour contractors and contractual systems in HIV prevention. 
AIDS 2008, 22, S127-S136. 

33. Tuan, N.A.; Fylkesnes, K.; Thang, B.D.; Hien, N.T.; Long, N.T.; Kinh, N.V.; Thang, P.H.; 
Manh, P.D.; O'Farrell, N. Human immunodeficiency virus (HIV) infection patterns and risk 
behaviours in different population groups and provinces in Viet Nam. Bull. World Health Organ. 
2007, 85, 35-41. 

34. Llacer, A.; Zunzunegui, M.V.; del Amo, J.; Mazarrasa, L.; Bolumar, F. The contribution of a 
gender perspective to the understanding of migrants' health. J. Epidemiol. Commun. Health 2007, 
61, ii4-iil0. 

35. Shedlin, M.G.; Drucker, E.; Decena, C.U.; Hoffman, S.; Bhattacharya, G.; Beckford, S.; 
Barreras, R. Immigration and HIV/AIDS in the New York Metropolitan Area. J. Urban Health 2006, 
83, 43-58. 

36. Castilla, J.; Sobrino, P.; del Amo, J. HIV infection among people of foreign origin voluntarily 
tested in Spain. A comparison with national subjects. Sex. Transm. Infect. 2002, 78, 250-254. 

37. Gras, M.J.; Weide, J.F.; Langendam, M.W.; Coutinho, R.A.; van den Hoek, A. HIV prevalence, 
sexual risk behaviour and sexual mixing patterns among migrants in Amsterdam, The Netherlands. 
AIDS 1999, 13, 1953-1962. 

38. Xiridou, M.; van Veen, M.; Coutinho, R.; Prins, M. Can migrants from high-endemic countries 
cause new HIV outbreaks among heterosexuals in low-endemic countries? AIDS 2010, 24, 
2081-2088. 

39. Wasserheit, J. Epidemiological synergy: Interrelationships between human immunodeficiency 
virus infection and other sexually transmitted diseases. Sex. Transm. Dis. 1992, 19, 61-77. 

40. Agha, S. Factors associated with HIV testing and condom use in Mozambique: Implications for 
programs. Reprod. Health 2012, 9, doi:10.1 186/1742-4755-9-20. 

41. Fenton, K.A. Sustaining HIV prevention: HIV testing in health care settings. Top. HIV Med. 2007, 
15, 146-149. 

42. Gilbert, PA.; Rhodes, S.D. HIV testing among immigrant sexual and gender minority Latinos in a 
US region with little historical Latino presence. AIDS Patient Care STDs 2013, 27, 628-636. 

43. Donker, G; Dorsman, S.; Spreeuwenberg, P.; van den Broek, I.; van Bergen, J. Twenty-two years 
of HIV-related consultations in Dutch general practice: A dynamic cohort study. BMJ Open 2013, 
3, doi:10.1136/bmjopen-2012-001834. 

44. Petroll, A.E.; DiFranceisco, W.; McAuliffe, T.L.; Seal, D.W.; Kelly, J.A; Pinkerton, S.D. 
HIV testing rates, testing locations, and healthcare utilization among urban African-American men. 
J. Urban Health 2009, 86, 119-131. 



Int. J. Environ. Res. Public Health 2014, 11 



8566 



45. De Luca, G.; Ponzo, M.; Andres, A.R. Health care utilization by immigrants in Italy. 
Int. J. Health Care Financ. Economics 2013, 13, 1-31. 

46. Dias, S.F.; Severo, M.; Barros, H. Determinants of health care utilization by immigrants in Portugal. 
BMC Health Serv. Res. 2008, 8, doi:10.1 186/1472-6963-8-207. 

47. Dias, S.; Gama, A.; Cortes, M.; de Sousa, B. Healthcare-seeking patterns among immigrants in 
Portugal. Health Social Care Commun. 2011, 19, 514-521. 

48. Fenta, H; Hyman, I.; Noh, S. Health service utilization by Ethiopian immigrants and refugees in 
Toronto. J. Immigr. Minor. Health 2007, 9, 349-357. 

49. Dias, S.; Gama, A.; Cargaleiro, H; Martins, M.O. Health workers' attitudes toward immigrant 
patients: A cross-sectional survey in primary health care services. Hum. Resour. Health 2012, 
10, doi:10.1 186/1478-4491-10-14. 

50. Priebe, S.; Sandhu, S.; Dias, S.; Gaddini, A.; Greacen, T.; Ioannidis, E.; Kluge, U.; Krasnik, A.; 
Lamkaddem, M.; Lorant, V.; et al. Good practice in health care for migrants: Views and 
experiences of care professionals in 16 European countries. BMC Public Health 2011, 11, 
doi: 1 0. 1 1 86/147 1 -2458- 1 1 - 1 87. 

51. Lammers, J.; van Wijnbergen, S.J.; Willebrands, D. Condom use, risk perception, and HIV 
knowledge: A comparison across sexes in Nigeria. HIV/AIDS 2013, 5, 283-293. 

52. Zafar, M.; Nisar, N.; Kadir, M.; Fatmi, Z.; Ahmed, Z.; Shafique, K. Knowledge, attitude and 
practices regarding HIV/AIDS among adult fishermen in coastal areas of Karachi. 
BMC Public Health 2014, 14, doi: 10. 1 1 86/1471-2458-14-437. 

53. McCoy, H.V.; Hlaing, W.M.; Ergon-Rowe, E.; Samuels, D.; Malow, R. Lessons from the fields: 
A migrant HfV prevention project. Public Health Rep. 2009, 124, 790-796. 



© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article 
distributed under the terms and conditions of the Creative Commons Attribution license 
(http://creativecommons.Org/licenses/by/3.0/).